Invasive wild deer exhibit environmental niche shifts in Australia: Where to from here?

Abstract Invasive species have established populations around the world and, in the process, characteristics of their realized environmental niches have changed. Because of their popularity as a source of game, deer have been introduced to, and become invasive in, many different environments around the world. As such, deer should provide a good model system in which to test environmental niche shifts. Using the current distributions of the six deer species present in Australia, we quantified shifts in their environmental niches that occurred since introduction; we determined the differences in suitable habitat between their international (native and invaded) and their Australian ranges. Given knowledge of their Australian habitat use, we then modeled the present distribution of deer in Australia to assess habitat suitability, in an attempt to predict future deer distributions. We show that the Australian niches of hog (Axis porcinus), fallow (Dama dama), red (Cervus elaphus), rusa (C. timorensis), and sambar deer (C. unicolor), but not chital deer (A. axis), were different to their international ranges. When we quantified the potential range of these six species in Australia, chital, hog, and rusa deer had the largest areas of suitable habitat outside their presently occupied habitat. The other three species had already expanded outside the ranges that we predicted as suitable. Here, we demonstrate that deer have undergone significant environmental niche shifts following introduction into Australia, and these shifts are important for predicting the future spread of these invasive species. It is important to note that current Australian and international environmental niches did not necessarily predict range expansions, thus wildlife managers should treat these analyses as conservative estimates.


| INTRODUC TI ON
Invasive species are one of the leading causes of ecological change and biodiversity loss worldwide (Doherty et al., 2016;Mack et al., 2000). Humans have facilitated the invasion, and subsequent spread, of non-native species to previously inaccessible areas and niches, and these species have then gone on to become invasive (Da Re et al., 2020;Hernandez & Parker, 2018;Tingley et al., 2014). Here, a niche is defined as the range of ecological conditions in which a species can maintain viable populations Srivastava et al., 2020;Valverde et al., 2011).
Factors such as propagule pressure can influence the probability of an invasive species' successful establishment in a novel environment (Prins & Gordon, 2014), while other mechanisms such as adaptation can allow a species to expand its environmental niche (Kolar & Lodge, 2001;Kumar et al., 2015;Lakeman-Fraser & Ewers, 2013;Simberloff, 2009;Tingley et al., 2014).
Understanding the degree to which species' environmental niches can change post-introduction provides insights into invasion processes and assists with predicting areas vulnerable to future spread (Braschler et al., 2019;Guisan et al., 2014;Jourdan et al., 2021;Peterson, 2011).
As niche characteristics are often different between native and invaded environments, a species' ability to rapidly adapt to a novel environment can increase their probability of invasion and their likelihood of successful colonization (Gallagher et al., 2010;Guisan et al., 2014;Peterson & Nakazama, 2008;Sakai et al., 2001). Many species have expanded into environmental conditions that are not present in their native range, which could occur due to using a greater portion of their fundamental niche, exploiting phenotypic plasticity, or adapting to new conditions and spreading, defined here as undergoing an environmental niche shift (Beaumont et al., 2009;Blackburn & Duncan, 2001;Guisan et al., 2014;Jourdan et al., 2021;Pearman et al., 2008). Understanding the niche shifts that have occurred in species between their native and invasive distributions may help with understanding further range expansion and invasion potential Gonzalez-Moreno et al., 2015).
Species distribution models (SDMs) are a standard method to predict habitat suitability and invasion risk (Santamarina et al., 2019;Tingley et al., 2014;Valverde et al., 2011). To fully understand invasion risk, it is important to model habitat suitability using a species' global invaded distribution. Because organisms may not use their entire potential (i.e., fundamental) niche, predicting suitable habitats based only on the native distribution can severely underestimate the potential for an invasive species' establishment or spread in a novel environment (Ahmad et al., 2019;Morehouse & Tobler, 2013;Srivastava et al., 2020;Tingley et al., 2014). When quantifying suitable habitat using SDMs, it is also important to consider habitat connectivity because suitable habitat may occur in areas nowhere near a species' site of introduction ), making it difficult or impossible for the species to expand into them.
For this reason, it is important to model habitat connectivity in conjunction with suitability (Dunstan & Johnson, 2007;Soberón & Peterson, 2005;Valverde et al., 2011). Here, we used SDMs and connectivity metrics to predict the invasiveness of a widespread group of introduced fauna.
Invasive deer often have significant economic impacts, posing risks to motor vehicles, and competing with livestock for feed (Jesser, 2005;Kusta et al., 2017;McLeod, 2009). Despite this, humans have successfully established populations of deer globally (King, 2005), largely for game. Many deer now have broad international distributions (Forsyth & Hickling, 1998) and, like other species introduced to novel environments, can adapt, spread, and become invasive. Because deer have been so widely introduced internationally, and so often become invasive (Forsyth & Duncan, 2001;Hall & Hill, 2005;Long et al., 2003), it is important to calculate their niche using worldwide occurrences, as they are likely to occupy a large proportion of their fundamental niche space (i.e., realized niche). Here, we modeled deer distributions in Australia using their worldwide environmental niches to predict likely suitable habitat in Australia.
Deer were introduced to Australia in the early 1800s by acclimatization societies for hunting and to make the landscape more familiar for colonists (Bentley, 1967;Roff, 1960). Of the 29 species of deer brought to Australia (Table 1), six have established free-living populations and increased in population size and range (Bentley, 1967;Moriarty, 2004). These species have successfully established in multiple ecosystems across Australia, and many deer species are negatively impacting local environments and economies (Burgin et al., 2014;Davis et al., 2016;English, 2007;Forsyth et al., 2012;Jesser, 2005). Predicting their future ranges is thus important for control and management.
To identify areas vulnerable to future invasion by deer in Australia, we created SDMs for the native and international ranges of the six established deer species. To examine if deer changed their environmental niches (i.e., had a niche shift) following their introduction into Australia, we quantified the extent of niche overlap between each species' international and Australian ranges. We predicted that species with broader international invasive distributions would exhibit fewer differences between their international range and their Australian distribution compared to those species with limited global distributions. We expected that species whose native range was most similar to available Australian habitats would have the largest potential for spread. Species that have exhibited niche shifts since being introduced to Australia may spread beyond habitat presently deemed suitable by our SDMs. While all species may have the capacity for further spread, those that have already had niche shifts may be less predictable in terms of their potential future distributions.

| Species records and environmental data
Species presence data for the six deer species that have established in Australia were obtained from open-access databases. Native range and international occurrence records were collected from the Global Biodiversity Information Facility (GBIF; "GBIF.org"), and Australian occurrence records were collected from the Atlas of Living Australia (ALA; "ala.org.au"). We supplemented Australian records with direct observations from "FeralScan", a citizen science platform to track feral deer observation records in Australia ("www.feral scan.org. au"). We also supplemented Australian records of chital deer (Axis axis) with occurrence records collected from 2017 to 2020 using direct observations and systematic sampling campaigns (e.g., spotlighting and camera-trap surveys) conducted by the authors (Pople, pers. obs.). We filtered imprecise records (a coordinate uncertainty >1 km) and ensured that this left at least 50% of the dataset and at Abbreviations: CE, critically endangered; DD, data deficient; E, endangered; EX, extinct in wild; LC, least concern; V, vulnerable.

TA B L E 1
The 29 species (and subspecies) of deer brought to Australia (the six with wild distributions are in bold), and the states where they occurred.
least 20 unique records per species to maintain an adequate sample size. We removed records when there was more than one within a  Table S1. These variables were global raster layers that were sourced at 1 km resolution, generalized from a finer resolution raster, or rasterized from detailed vector data. For the niche overlap methods, we removed all predictor variables that were highly correlated (Pearson correlation coefficient >.80) to reduce multicollinearity. We were left with 16 variables (Table S2). For MaxEnt modeling, the entire full set of global environmental rasters (20 variables) were used, regardless of collinearity.

| Niche overlap methods
To estimate climatic niche overlap between the native and Australian ranges of the six deer species, we used the ecospat package (Broennimann et al., 2021;R Studio Team, 2017

| Maxent modeling methods
To model habitat suitability for each of the six deer species in Australia, we constructed species distribution models using maximum entropy (MaxEnt V. 3.4.0) modeling. MaxEnt uses occurrence records and "background" data points to estimate the probability of the presence of a species, generating an index of suitable habitat from 0 (lowest suitability) to 1 (highest suitability; Elith et al., 2011;Philips et al., 2006). We used a target background that is based on were then re-run, using these variables and 10-fold cross-validation.
The average area under the receiver operating characteristic curve (AUC; i.e., indications of model performance) was based on this latter run. We then used the "Fixed cumulative value 10" threshold from the MaxEnt output for each species to set a threshold for discriminating suitable from non-suitable habitat. This threshold was selected in an attempt to capture even marginally suitable habitat, as invasive species can expand their realized niche into non-suitable areas that would not have been identified using stricter thresholds.
Other than using a target background and variable selection, default MaxEnt settings were used. While tuning individual species models is generally advised, we kept the parameters constant to better compare results between our deer species.
To identify dissimilarity in suitability between the native range of each deer species and its range in Australia, we applied multivariate environmental similarity surface analyses (MESS; Elith et al., 2010).

MESS analysis allows visualization of the similarity between pixels
predicted to be suitable in Australia (as determined from the MaxEnt modeling), compared with conditions at known occurrences in the native range. A positive MESS value represents a pixel where there is high similarity between occupied native habitat and invaded habitat, and a negative value indicates dissimilarity between native and invaded habitats Elith et al., 2010). Note that MESS is often used to assess the suitability of MaxEnt models to project habitat suitability across novel climates. This is not the case here, as native and invasive ranges were both used for model training. Rather, MESS analyses were used here separately from MaxEnt models to assess dissimilarity between native and invaded environments.
To determine where the six deer species in Australia are likely to spread in the future, we created invasion risk maps derived using the suitable habitat layer (established from the MaxEnt modeling) and current deer ranges. To determine if deer could spread to new areas, we calculated cost distances from known occurrences using the R function accost() from the package gdistance (Etten, 2017), which calculates the "accumulated distance" using habitat suitability as a cost surface. This analysis assumes that species are more likely to spread to cells with greater suitability estimates from points of known occurrence. These cost distance values are used to down-weight values from the initial suitability map such that areas far away and difficult to reach have small invasion risk values even if their initial suitability values are high. We then scaled these values from 0 (very far and hard to invade) to 1 (near known occurrences and high invasion risk).
To determine the area in which species are predicted to spread, we removed areas that were already occupied by deer, and this area was calculated using the α-hull methodology (Burgman & Fox, 2003) in the alphahull package (Pateiro-Lopez & Rodriguez-Casal, 2019). We applied an α-hull value of 1.5 to all species. Using the Australian occurrence records of each species, we generated maps of each deer's present range and overlaid those with maps of invasion risk (i.e., removed the area that was already occupied by the deer).

| Niche shifts
We found evidence of niche shifts in some species, with low niche overlap values when we made pairwise comparisons of each species' international and Australian ranges (D = 0-0.292; Table 2; Figures S1-S6). Hog, rusa, sambar, and fallow deer exhibited relatively large niche shifts, and thus underwent significant niche expansion following introduction to Australia ( Figure 1; Table 2). In contrast, the ranges of chital and red deer in Australia are enclosed within the total niche envelope of their international ranges, exhibiting limited niche expansion (0.007 and 0.134, respectively) and high stability (0.993 and 0.866, respectively). Despite this, niche similarity between international and Australian ranges of red deer was still not statistically significant (p = .150). There was significant similarity between the international and Australian niches of chital deer (p < .001). Fallow deer also exhibited relatively high niche stability (0.892; Table 2) although, unlike chital or red deer, fallow deer had some degree of niche expansion (Table 2). Hog deer exhibited no niche overlap between international and Australian ranges ( Figure 1c) and thus showed no niche stability (0.000) and high niche expansion (1.000).
Species niche profiles for each variable were also quantified (Figures S7-S12), with maximum temperature in the warmest month, minimum temperature in the coldest month, and average annual rainfall selected to compare international and Australian ranges of deer (

| Habitat suitability modeling and present ranges
Our models predicting the future suitable habitat of deer in Australia performed well; AUC values for all species were >0.85 ( Figure S13).
Contributing variables are also presented in Table S3. Of all deer species examined here (Figure 2) Figure S14.

| DISCUSS ION
Five of the six deer species introduced to Australia (fallow, hog, red, rusa, and sambar deer) occupy significantly different niches in Australia compared to their international niche profiles (Figure 1). F I G U R E 2 Maps of invasible habitat and future spread range from high vulnerability (brown) to low vulnerability (teal) as determined by MaxEnt modeling, including records (dots) of the six feral deer species in Australia. For maps including the present range polygons, see Figure S14.

Chital deer Hog deer
Fallow deer Red deer Sambar deer Rusa deer have already spread beyond habitats typical of their international niches. In contrast, chital, hog, and rusa deer have the potential to spread much further than their present distributions. Of all the species examined, chital deer have the greatest predicted range in Australia, orders of magnitude greater than the other species. As such, chital deer potentially represent a management problem following invasion in northern and eastern Australia.
In the future, deer in Australia are likely to expand their current distributions (Figure 2). Fallow deer are currently spreading north from their current distributions in Victoria and New South Wales, beyond habitat predicted to be suitable, and establishing in areas that are warmer than the international range. Likewise, red deer are present in areas that are warmer, but also wetter than where they occur outside Australia. Hog and rusa deer have shifted into drier and colder ranges following introduction to Australia. Hog deer have a high degree of potentially invasible habitat north of their current distribution in Victoria, and it seems likely that they will spread into this area. Rusa deer are expanding south along the south-eastern coast of Australia. Finally, sambar deer are predicted to spread further north along the north-eastern coast from their present range. Many of these invasible areas represent valuable agricultural and conservation areas. Deer in Australia are already competing with livestock for forage and feeding on crops (Bentley, 1998;Davis et al., 2016). Deer invasions into natural areas are likely to cause degradation of water quality through trampling, erosion, and increased nutrient loading (McDowell, 2007(McDowell, , 2008. Impacts of deer are likely to increase in these sectors as deer populations continue to grow and spread beyond their present distributions. As populations increase in size, genetic variation should also increase, which facilitates evolution and adaptation to new environments (Lee, 2002;Urban et al., 2007). Likewise, as yet unrealized phenotypic plasticity could allow populations of invasive species to expand quickly (Davidson et al., 2011). Population expansion can drive individuals into suboptimal habitats, thus forcing animals to face novel environmental conditions (Hardie & Hutchings, 2010;Urban et al., 2007). Even without adaptation, chital, hog, and rusa deer have the capacity to spread beyond their current distributions.
Considering the ability of these species to exhibit niche shifts, it is F I G U R E 3 Habitat suitability predicted from native and introduced ranges of the six deer in Australia. Symbology bar indicates similarity with dark blue indicating high similarity (100%) and dark brown indicating low (−100%). Based on our models, chital deer have the capacity to spread further from their present distribution than the other five species in Australia (Table 4). There were no significant differences between niches in the international and Australian ranges for chital deer, probably because they were introduced to habitat similar to their native range (Figure 3a). Compared to the other deer species in Australia, chital deer have not had to adjust to a particularly novel environment ( Figure 3). Since their present distribution is relatively restricted compared with other deer species in Australia, population spread may be limited by other biotic or abiotic variables (Kelly et al., 2021;Watter et al., 2019). Despite this, chital deer represent a significant risk in the Australian environment, because much of the present habitat adjacent to their current distribution is ecologically similar to their native range. They are likely to spread even without any intrinsic changes in their habitat requirements.
In contrast to chital deer, the other five species of deer in Australia have exhibited significant niche shifts since arriving.
As many of the deer species in Australia have broad international ranges (except for hog deer), international ranges likely represent something akin to their fundamental niche, and the observed spread into new niche space in the Australian environment likely represents true niche shifts. Many invasive species undergo rapid evolution following invasion, quickly adapting to conditions in the novel environment (Broennimann et al., 2007;Callaway & Maron, 2006;Maron & Alexander, 2014), which we believe has likely occurred in several deer species introduced into Australia.
Hog deer have a very limited history of introduction worldwide, and their invaded range is almost completely confined to Australia (Hill et al., 2019). Prins and Gordon (2014) proposed that a species will not invade areas with abiotic conditions outside its physiological tolerance levels. If we accept this theory, then these Australian ecosystems must fall within their physiological tolerance. The success of hog deer in Australia demonstrates that species with limited native or worldwide distributions can spread beyond predicted ranges, simply because we do not know their physiological tolerances. In addition, physiological tolerances can evolve (Lee et al., 2003;Qu & Wiens, 2020) and invasive species can exhibit a high degree of phenotypic plasticity (Davidson et al., 2011). Even with accurate knowledge of physiological tolerances, the accuracy of predictions of spread may be limited.
While habitat suitability has certainly contributed to the success and spread of invasive deer in Australia, the number of deer introductions, or propagule pressure, has also likely played a role (Fautley et al., 2012;Forsyth et al., 2004). Propagule pressure influences establishment success, as well as subsequent viability of a population (Forsyth & Duncan, 2001;Leung et al., 2004;Lockwood et al., 2005;Prins & Gordon, 2014 Sutherst et al., 1999) often occurs on a much coarser scale than species distribution modeling due to the available settings and limited customization of predictor variables, thus overestimating the potential range of invasive species (Elith et al., 2011;Froese, 2012;Kumar et al., 2015;Srivastava et al., 2019;Wearne et al., 2013). Because of the more detailed response, the complexity of MaxEnt for habitat suitability modeling allows more accurate predictions of the future distribution of invasive species, compared with previous methods.
Deer have had the opportunity to invade, and subsequently adapt to, many areas around the world. As such, we might expect that many deer species have had the opportunity to fill their entire TA B L E 4 Total area (km 2 ) presently occupied (present range) and uninvaded habitat, calculated from Figure 2. Note: The % difference represents the area between the present range and the threatened range that has not yet been invaded. environmental niche. Here we demonstrate that five of the six deer species introduced to Australia showed significant shifts in their environmental niches, and three have already spread beyond their predicted suitable habitat. As deer continue to move into different environments, it is likely that they will continue to adapt to previously unavailable niches, thus increasing their potential for future spread, not only in Australia, but worldwide. If this continues, then these pest species will be far more problematic and widespread than we can predict using SDMs alone. writing -original draft (equal); writing -review and editing (equal).

ACK N OWLED G M ENTS
We are extremely grateful to Peter West, FeralScan, and the Centre for Invasive Species Solutions for the generous use of their data of Australian deer records. This manuscript was edited by Caley Editorial Services.

FU N D I N G I N FO R M ATI O N
This manuscript was partially funded through an ARC Linkage grant to BTH (LP1801000267). We thank DAF Queensland and JCU for additional support.

CO N FLI C T O F I NTER E S T S TATEM ENT
The authors declare no conflict of interest.

DATA AVA I L A B I L I T Y S TAT E M E N T
Occurrence records from ALA and GBIF and environmental data are available on the relevant referenced publicly available databases.
Occurrence records from FeralScan were collected and used in agreement with Peter West and FeralScan and are not publicly available.